Category: natural selection

On the origin of venom by means of natural selection

December 11, 2025 • 10:20 am

Many animals are venomous, but in most cases the exact proteins involved in causing pain or death are unknown, and even in those cases the genes producing them have not been identified, counted or mapped.  If you’re interested in the evolution of venom, what its precursors are, and how venomous animals avoid poisoning themselves, you have to know this kind of stuff.

A new paper in Proc. Nat. Acad. Sciences (click screenshot below to read for free, or find the pdf here) answered several of these questions in the venomous caterpillar of the mottled cup moth (Doratifera vulnerans), shown below.  It’s from Australia, and is described in Wikipedia this way:

It is known for its caterpillar having unique stinging spines or hairs that contain toxins, for which the scientific name is given that means “bearer of gifts of wounds”. Chemical and genetic analysis in 2021 show that its caterpillar contains 151 toxins, some of which have medicinal properties

That earlier paper, from 2021 and including some of the same authors as the one we discuss today, did indeed identify 151 proteins (peptide are bits of proteins or short chains of amino acids) that were in the toxins, but did not know which genes produced them, how the genes were arranged, what the closest relatives of the genes were, and how many of the 151 “toxins” were really toxic (the word “toxin” there and in the present paper do not mean that the substances were toxic, but that they were simply a component of the extracted toxins). However, the authors, some on the paper I’m highlighting today, did identify two genuine toxins that caused pain: the peptides Dv12 and Dv11.

Look at this thing! It’s clearly aposematic, meaning that it has bright warning coloration that predators can recognize and learn to avoid. And you can see those nasty spines.  In the earlier paper they extracted toxins from related species and tested them by injecting them into mice tails, guinea pigs, and human volunteers. That earlier paper also adds this about the species name:

This species, whose binomial name etymologically means “bearer of painful gifts,” is a common culprit of caterpillar envenomations in Australia.

That means that many Aussies get stung by these things, probably inadvertently. Would you touch an animal that looks like this?:

Photo by Fir0002,  Creative Commons Attribution-Share Alike 3.0 Unported license.

On to the new paper, and I’ll try to be brief as it’s long and complicated.

1.) First, the authors sequenced the entire caterpillar genome (remember, it’s the same as the adult moth genome).

2.) Then, knowing the sequences of the proteins known from previous work on toxins, they could find the genes producing them by matching the protein sequence to the DNA sequence that could produce these proteins. Of the 151 proteins in caterpillar venom known from the prvious work, they mapped 149 of them to 115 sites in the genome

3.) Of the 115 sites, 35 were products of single genes, while 80 (70%) of the total, were members of gene families consisting of two or more similar genes (sometimes many genes) with similar sequences.  Here’s a map of the “toxin gene” locations on the insect’s 13 chromosomes. The blue dots are the genes existing in single copies, orange dots are clusters of genes previously grouped together by protein-sequence similarity, and pink dots are genes that were newly identified, surely as part of gene families, in the present study. This conclusion comes from their sequence similarity and they physical grouping on two chromosomes.(The size of the dots indicates the number of genes that are part of a contiguous group. Click to enlarge:

So we know that genes found in venom are very often the product of gene duplications, either of single genes becoming two (this can happen via unequal crossing-over during meiosis or by other methods), producing two initially identical genes side by side or whole groups of them (“tandem duplications”). Once a gene has been duplicated, the original copy can then keep its original function, while the other copies, not being “needed,” are free to evolve other functions. Many genes we’re familiar with, like our own globins and immunoglobulins, evolved by gene duplication followed by divergence of the duplicated copies.

Where did the genes making venom proteins come from? This is the key evolutionary question answered here and, to some extent, in the previous paper. They evolved from ancestral genes in the moth’s immune system that evolved to attack microbes, the so-called “antimicrobial peptides” (AMPs), also known as cecropins. The ancestral AMP proteins, nearly identical to their original form and function, kill bacteria (prokaryotes) by disrupting the bacterial membranes. Insects still need to kill microbes!

Clearly, the proteins in venom have evolved by natural selection modifying ancestral genes used to kill bacteria. Now they are used to repel predators. Natural selection causing this divergence was implicated by looking at sequence differences, as there are ways of showing what sequence differences evolve faster than expected under either the slower processes of genetic drift or “purifying” selection that conserves structure.  They found that most of the venom-adapted proteins that evolved from cecropins did evolve under natural selection, while the descendants of cecropins that retained their original anti-microbial proteins were under purifying selection to retain their sequence. It’s clear, then, that the insect still needs genes to attack bacteria. It’s just that some of them have been repurposed, often through gene duplication and divergence, to repel predators. (The authors have a way of assessing “pain” by measuring the increase in calcium concentration in cells grown in vitro and exposed to venom. This happens when the two investigated proteins are used.)

Here is a complicated family tree of cecropin genes in black used to kill microbes. The genes found in venom are in the red box (“venom adapted”). You can see that they are related to cecropin genes but branched off fairly recently (probably four or five million years ago). The venom genes are in the red box that I’ve added, and their relationship as being derived from ancestral AMP genes is very clear. (The “canonical” genes in green are antimicrobial proteins closely related in sequence to the venom genes.

So, now we know where the genes in venom come from. What we do not know is how many of those genes are essential in venom, either causing pain or doing other stuff that venom needs to do. At least two of them cause pain, but there are probably more, for they haven’t all been tested. And some of the other genes are probably involved in dismantling cell walls in potential predators. The authors tested several of the venom proteins and also found that, as in their AMP ancestors, they disrupt cell covering, in this case eukaryotic cell membranes.

Finally, the big question: If the caterpillar makes venom, why doesn’t it poison itself? Here’s how the authors answer that question (I’ve put the answer for this species is in bold).

Animals that produce toxins, either for innate immunity or as venom toxins, must employ strategies to protect themselves from toxicity. Such protective mechanisms include production of toxin inhibitors, storage in inactive form, mutations in their own ion channels that confer resistance, alteration of lipid bilayer compositions, and compartmentalization of toxins separate from body tissues. In the case of limacodid venom peptides, the venom is compartmentalized into the cuticle-lined venom reservoir inside venom spines, preventing the toxin from coming into contact with cells other than the secretory cells that produce them. Thus, compared to canonical cecropins, venom-adapted cecropins may also be released from pressure to avoid activity against animal cells.

There are other findings in the paper that will be of interest primarily to those studying genomic evolution. For example, many of the venom proteins still retain some weak antimicrobial activity, so the idea that genes completely lose their ancestral function when they gain a new one doesn’t hold in this case.

Below you can see the adult moth because, remember, they studied caterpillar venoms, and many of those genes are probably turned off in the adult. But adult and caterpillar carry the exact same genes, of course; their different bodies, physiology, and behavior rest on the differential turning on and off of these genes at different life stages. And that remains a big mystery: how do such different life stages evolve, with each step of the evolution being adaptive?

From The Australian Museum, photo credits at bottom (click to enlarge), image by Lyn Craggs.

 

Michael Lynch takes apart two attempts to forge new evolutionary “laws”

June 13, 2025 • 10:00 am

Biology isn’t really like physics: we don’t have “laws” that are always obeyed, but instead have generalizations, some of which hold across nearly organisms (but even the “law” that organisms have DNA as their genetic material is flouted). The only “law” I can think of is really a syllogism that Darwin used to show natural selection: a). if there is genetic variation among individuals for a trait, and b). if carriers of some of the variants leaves more copies of their genes for the trait than carriers of other variants, then c). those genes will be overrepresented in future generations, and the trait will change according to the effects of the overrepresented genes.

But even that is not a “law” but a syllogism. After all, natural selection doesn’t have to work.  There may be no genetic variation, as in organisms that are clonal, and different variants may not leave predictably different copies of themselves in future generations; such variants are called “neutral”.  So there is no “law” that natural selection has to change organisms.

In this paper (click on screenshot below, or find the pdf here), evolutionary geneticist Michael Lynch from Arizona State University goes after two papers (cited at bottom of this post) that, he says, are not only failed attempts to concoct “laws” of evolution, but are flat wrong because their proponents don’t know squat about evolutionary biology.  I’ll try to be very brief because the arguments are complex, and unless you know Lynch’s work on the neutral theory, much of the paper is a tough slog.  What is fun about the paper, though is that Lynch doesn’t pull any punches, saying outright that the authors don’t know what they’re doing.

Here’s the abstract followed by an early part of the paper, just to show you what Lynch is doing. Bolding is mine:

Abstract:  Recent papers by physicists, chemists, and geologists lay claim to the discovery of new principles of evolution that have somehow eluded over a century of work by evolutionary biologists, going so far as to elevate their ideas to the same stature as the fundamental laws of physics. These claims have been made in the apparent absence of any awareness of the theoretical framework of evolutionary biology that has existed for decades. The numerical indices being promoted suffer from numerous conceptual and quantitative problems, to the point of being devoid of meaning, with the authors even failing to recognize the distinction between mutation and selection. Moreover, the promulgators of these new laws base their arguments on the idea that natural selection is in relentless pursuit of increasing organismal complexity, despite the absence of any evidence in support of this and plenty pointing in the opposite direction. Evolutionary biology embraces interdisciplinary thinking, but there is no fundamental reason why the field of evolution should be subject to levels of unsubstantiated speculation that would be unacceptable in any other area of science.

. . . we are now living in a new kind of world. Successful politicians and flamboyant preachers routinely focus on the development of false narratives, also known as alternative facts, repeating them enough times to convince the naive that the new message is the absolute truth. This strategy is remarkably similar to earnest attempts by outsiders to redefine the field of evolutionary theory, typically proclaiming the latter to be in a state of woeful ignorance, while exhibiting little interest in learning what the field is actually about. Intelligent designers insist that molecular biology is too complex to have evolved by earthly evolutionary processes. A small but vocal group of proselytizers clamoring for an “extended evolutionary synthesis” continues to argue that a revolution will come once a critical mass of disciples is recruited (7–9), even though virtually every point identified as ignored has been thoroughly evaluated in prior research; see table 1.1 in ref. 6. More than one physicist has claimed that all of biology is simply physics. But 2023 marked a new level of advocacy by a small group of physicists, chemists, and geologists to rescue the field of evolutionary science from obfuscation, and to do so by introducing new theories and laws said to have grand unifying potential.

Note Lynch’s criticism of the “Extended Evolutionary Synthesis”, a program (and associated group of investigators) who claim revolutionary ways of looking at evolution, which, as Lynch notes, have already been discussed under conventional neo-Darwinian theory.

There are two theories Lynch criticizes in this paper

1.) Assembly theory. This is the complicated bit from the paper of Sharma et al. (see references below). It involves an equation that supposedly gives a threshold beyond which the assembly of components indicates life that evolved via natural selection (I won’t define the components, either, which aren’t important for the general reader’s purpose:

According to Walsh, this equation is totally bogus because it neglects all the forces that can impinge on gene forms during evolution. An excerpt:

However, this is not the biggest problem with assembly theory and its proposed utility in revealing the mechanistic origins of molecular mixtures. A second, more fundamental issue is that the authors repeatedly misuse the term selection, failing to realize that, even in its simplest form, evolution is a joint function of mutation bias, natural selection, and the power of random drift. There is a fundamental distinction between the mutational processes that give rise to an object and the ability of selection (natural or otherwise) to subsequently promote (or eradicate) it. In the field of evolution, drift refers to the collective influences of stochastic factors governed by universal factors such as finite population size, variation in family sizes, and background interference induced by the simultaneous presence of multiple mutations; via the generation of noise, the magnitude of drift modulates the efficiency of selection. For the past century, these processes have been the central components of evolutionary theory (reviewed in refs. 5 and 6).

Because this theory neglects forces like mutation and genetic drift that can change frequencies of gene forms beyond natural selection, Lynch deems it “a meaningless measure of the origins of complexity.”

2.) The notion that organismal complexity is an inevitable result of natural selection. This goes after the paper of Wong et al., and you should already know that this can’t be true: evolution is not, in any lineage, a march towards more and more complex species. The immediate refutation is the existence of parasites like fleas and tapeworms, which have lost many of their features to pursue a parasitic lifestyle.  If you make your living by parasitizing other organisms, natural selection can actually favor the loss of complexity. Tapeworms, for example, have lost many of their sensory systems, their digestive system, and features of their reproductive system.  By any measure of complexity, they are much simpler than their flatworm ancestors.

Lynch points this out, and adds that there are lineages of microbes (very simple one-celled organisms like bacteria) that have not become more complex over the billions of years they existed. There may have been a burst of complexity when the lineages arose, but clearly bacteria haven’t been on a one-way march to primates. They are doing a fine job as they are:

Despite their substantially more complex ribosomes and mechanisms for assembling them, eukaryotes do not have elevated rates or improved accuracies of translation, and if anything, catalytic rates and degrees of enzyme accuracy are reduced relative to those in prokaryotes (with simpler homomeric enzymes). Eukaryotes have diminished bioenergetic capacities (i.e., growth rates) relative to prokaryotes (21, 22), and this reduction is particularly pronounced in multicellular species (23). Finally, it is worth noting that numerous organisms (parasites in particular, which constitute a large fraction of organisms) typically evolve simplified genomes, and many biosynthetic pathways for amino acids and cofactors have been lost in the metazoan lineage.

Another bit of evidence against Wong et al. is that their adducing “subfunctionalization”, whereby genes duplicate and the duplicate copies assume new functions, shows some “law” of increasing complexity. (The divergence of hemoglobins occurred in this way.) But Lynch suggests that genes don’t duplicate to make an organism more complex, and, moreover, the differential functions of duplicate genes can arise from selection being relaxed:

Subfunctionalization does not arise because natural selection is striving for such an endpoint, which is an energetic and a mutational burden, but because of the relaxed efficiency of selection in lineages of organisms with reduced effective population sizes. How then does one relate gene number to functional information?

Lynch winds up excoriating these new “theories” again:

For authors confident enough to postulate a new law of evolution, surely some methodology and supportive data could have been provided. Science is littered with historical fads that became transiently fashionable, only to fade into the background, with a nugget of potential importance sometimes remaining (e.g., concepts derived from chaos theory, concerted evolution, evolvability, fractals, network science, and robustness). But usually when the latter happens, there is a clear starting point. This is not the case with the “law of increasing functional information,” which fails to even provide useful definitions of function and information.

. . . . To sum up, all evidence suggests that expansions in genomic and molecular complexity, largely restricted to just a small number of lineages (one including us humans), are not responses to adaptive processes. Instead, the embellishments of cellular complexity that arise in certain lineages are unavoidable consequences of a reduction in the efficiency of selection in organisms experiencing high levels of random genetic drift.

I would take issue only with Lynch’s claim that only a “small number of lineages” have become more complex than their ancestors.  Most multicellular organisms are this way.  In the end, though, Lynch’s lesson is that people should learn more about evolutionary theory, which has grown quite complex, before they start proposing “revolutionary laws of evolution.”

The two papers at issue (I’ve provided links.)

10. A. Sharma et al., Assembly theory explains and quantifies selection and evolution. Nature 622, 321–328 (2023).

11. M. L. Wong et al., On the roles of function and selection in evolving systems. Proc. Natl. Acad. Sci. U.S.A. 120, e2310223120 (2023). 

Possible evolution of hummingbird beaks since WWII

May 28, 2025 • 10:45 am

The report below may represent a case of rapid adaptive evolution of a trait: the beaks of Anna’s hummingbirds (Calypte anna) in California, though there are sufficient confounding factors that, were I teaching evolution, I would still use Peter and Rosemary Grant’s work on the beaks of medium ground finches in the Galápagos as my paradigm. (The Galápagos incident occurred over a single year on one small island and confounding factors are virtually nil).

First the species: a male Anna’s Hummingbird flying:

Robert McMorran, United States Fish and Wildlife Service, Public domainvia Wikimedia Commons

and a female hovering:

Mfield, Matthew Field, CC BY-SA 3.0 via Wikimedia Commons

Click below to read the article, and find the pdf here.

The authors posited that the increasing use of hummingbird feeders after WWII would select for changes in the bill length of this species because individuals who could reach and consume more nectar from newfangled feeders (which reward copious nectar swilling) would have a reproductive advantage. Their predictions were met, but there are complications.

Here’s a hummingbird feeder:

Centpacrr at English Wikipedia, CC BY-SA 3.0, via Wikimedia Commons

That’s a very common design, with the feeder filled with sweet liquid: often sugar water, which is okay but commercial nectar containing other nutritive substances is better. The paper describes the spread of feeders and the morphology of AH beaks over time, using about 400 museum specimens gathered since 1860. Feeders, though, were introduced mostly after WWII (from the paper):

Although it likely existed earlier, we report that the widespread recreational hummingbird feeding can be traced back to an article published in National Geographic in 1928 documenting how to ‘tame’ hummingbirds by making bottles of sweet liquid masquerading as flowers (Bodine 1928); this method is thought to have directly influenced the first patented hummingbird feeder in 1947 (True 1995). As a result of this newly popularized feeder, terms associated with hummingbird feeders in local newspapers increased rapidly from southern to northern California, where feeder density began its increase in the historic range accompanied by an increase of ANHU populations as they moved north.

Based on the spread of hummingbird feeders, the authors posited an evolutionary change in beak shape (remember, this is over 80 years):

We therefore expect feeders to select for increased volume with each lick resulting from increased bill length and thickness. In feeders, unlike flowers, nectar pools are not quickly depleted and therefore the short distance between the bill tip and the nectar surface remains relatively constant, such that minimizing the bill-nectar gap allows higher licking rates and extraction efficiency (Kingsolver and Daniel 1983; Rico-Guevara et al. 2015; Rico-Guevara and Rubega 2011; Kingsolver and Daniel 1983).

“Minimizing the bill-nectar gap” involves evolving longer bills. And getting more capacious bills allows you to take in more nectar in one slurp.

And this is what they found.  First, though, there are quite a few confounding factors that the authors had to consider:

  • Eucalyptus trees, an invasive species and also a source of food for Anna’s Hummingbird (called AH in this post), also spread over that period
  • Humans also spread, and urbanization spread from southern to northern California, so there is a climatic factor to consider, too. Since bills are a source of heat loss, we expect birds in colder climate sin the north to have shorter bills (and they did indeed find this)
  • Feeders could have a secondary effect by promoting fights between males, who try to monopolize the “nectar” source. It could be this fighting that would select for changes in bill shape, since bills are used in fighting. Attendant changes in female shape could simply be a byproduct of selection in males.
  • Increased urbanization itself could change beak shape, perhaps because it leads to planting of flowers that select for longer bills

Data analysis was done (this is above my pay grade) using a multivariate analysis, taking into account year, location, temperature, beak measurements, and the abundance of feeders and Eucalyptus trees. The latter two factors were estimated—not very satisfactorily—using newspaper mentions since 1880. The results were these:

  • The abundance of eucalyptus trees had a small effect on increasing bill length and thickness, but it was much smaller than. . . .
  • The density of feeders, which had a highly significant effect, increasing both bill length and thickness (bill dorsal area) in the predicted way
  • However, bill size was smaller in colder climates, representing a presumed tradeoff between acquiring nectar from feeders and conserving heat when it’s cold
  • Human population size and year also had strong effects, changing the trait in the expected direction, as one would expect if natural selection were causing evolution of bill size and shape over time
  • Feeder density had a stronger effect on population size of AHs in northern rather than southern California. From the paper:

We find that feeders and human population size are both strongly positively associated with ANHU [Anna’s Hummingbird] counts (Figure S9) and each appear to have facilitated population growth differently throughout California (Figure 1B,C). Specifically, feeder availability appears to have facilitated population growth at northern latitudes, whereas human population size appears to have contributed more strongly to population growth in ANHU’s native range in southern California. These findings corroborate work conducted by Greig et al. (2017) suggesting that hummingbirds at northern latitudes are more reliant on feeders in winter than those at southern latitudes, while ANHU population growth is supported by urbanized human environments.

Why urbanized environments select for higher hummingbird populations independently of feeders is a bit counterintuitive, but perhaps it has to do with planted gardens.

The upshot:  So, do we have an example of evolution by natural selection here, one based on the proliferation of feeders causing evolution in beak length and shape? It’s possible, but there are a lot of problems. They include a rather small sample size for a model with many covarying factors, the use of newspapers to estimate feeder and Eucalyptus density, an unexplained change in beak shape with feeder density (a constriction appears in the middle of the beak), and no solid evidence that the change is really genetic rather than a change in beak shape induced environmentally by the use of feeders.  (I’ll add, though, that increasing change in time suggests genetic evolution rather than a one-time environmental modification by using feeders.) But the Grants’ work had pretty strong evidence that the change in beak size in the Medium Ground Finch on Daphne Island was genetically based. (They did a heritability analysis.)

One way to test this hypothesis would be to take an area lacking many feeders, but having Anna’s Hummingbirds, and then saturate it with feeders (best to use commercial nectar). If you monitor the birds over a number of years, one should expect to see, in that one small area, a change in beak shape. But nobody is going to do this experiment, because they’d probably expire before it was done. The Grant’s experiment documented change in beak shape over just a single year, and is, to me, far more convincing.

The fantastic Alpine ibex, and some musings about the primacy of behavioral adaptation

January 27, 2025 • 12:15 pm

I’m feeling grotty today, probably because of dysthymia compounded by lack of sleep. I hope to be okay tomorrow, but in the meantime we have show and tell. The show and tell today involves the Alpine Ibex (Capra ibex), the subject of a nice seven-minute video.  It concentrates on their remarkable ability to climb on ledges that look unclimbable, something the many goat species can do as well.  The videos mentions that young goats must “overcome their fear,” but I wonder if they really feel fear.

Note the morphological traits that have evolved in concert with this behavior, including body shape. Surely the ability to climb (a behavioral trait) preceded the evolution of things like those split hooves with soft pads, supporting Ernst Mayr’s claim that many key adaptations begin not as changes in morphology, but changes in behavior that give a premium to later morphological evolution. I just opened a book that was perhaps the most influential volume of my career, Mayr’s 1963 Animal Species and Evolution. I found this sentence on p. 604:

“A shift into a new niche or adaptive zone is, almost without exception, initiated by a change in behavior.”

Mayr was a smart guy, and was probably right. The important question, though, is, though, “do those changes in behavior have a genetic basis“? It’s hard to see, for example, how a goat with a greater propensity to climb, but not one based on genetic differences from other individuals, could possibly kick off a bout of evolutionary change, for there would be no increase of climbing behavior unless it came with an adaptive advantage that could be passed on via genes.  If the first climbers did have genetic differences from non-climbers, and climbing resulted in more of your genes being passed on, you would get an increase in the behavior over time since it conferred a reproductive advantage. (This didn’t start with some individuals climbing sheer cliffs, of course!). After that, any mutations changing the hoof or body shape would be subject to natural selection.  In this case, simple behavioral variation not based on genes wouldn’t, I think, kick off behaviors and morphologies like those shown below.

I can think of one exception: the famous case of cultural evolution of milk-drinking in British birds, first noted by Fisher and Hinde in 1949 (they studied blue and great tits). This was apparently a case of cultural evolution, which started with one or a few individuals prying the tops off milk bottles left on doorsteps and drinking the cream. This spread rapidly throughout the UK, so rapidly that it must have been a spread via imitation—that is, cultural evolution, not genetic evolution. Of course that would be followed by natural selection leading to things like prying the caps off better (beak changes?), locating milk bottles more readily, and digesting the milk. I don’t think anybody has studied any subsequent evolution in the birds (for one thing, milk isn’t delivered on doorsteps any more!); but this is one case in which a potential change in an “adaptive zone”—however you describe it—began with a simple behavioral change not based on genetic differences.

Sorry, I was just thinking on paper. Watch the video, which is amazing and instructive:

ZeFrank on plants with explosive dispersal

July 1, 2024 • 12:20 pm

There’s a trigger warning on ZeFrank’s recent video: “True Facts is not appropriate for children, nor for adults who don’t act like children.” But in fact this 11+ minute video is perfectly appropriate for kids. (There’s a commercial from 3:15 to 4:22).

It’s about plants that disperse their seeds, spores, or pollen explosively, including liverworts, dogwoods, mosses, witch hazel, oats, and sundry others.

Not only do the explosions disperse the seeds (clearly an adaptive trait; you want your genes to be away from your plot, where they compete with you), but in some cases the explosion has evolved to give the dispersing seeds an orientation that makes them go further.  And some of the spores, as in horsetails, have little arms that curl with changes in humidity that allow them to “walk” along the ground! (Oat seeds can do the same thing, hopping with their “awns” and then twisting themselves into the ground.) As usual, the photography is amazing, so don’t miss this one. The extensive research is documented by a list of references at the end.

In this video ZeFrank doesn’t mention evolution or natural selection, but of course it’s implicit in these amazing and diverse adaptations for dispersal. I, for one, hardly knew anything about these features, and was delighted to see all these complicated results of natural selection, which of course is cleverer than you are.  Seeds that plant themselves by screwing themselves into the dirt!

h/t: Mary

How did warning coloration evolve?

June 5, 2023 • 9:30 am

Aposematic coloration, often called “warning coloration”, is the presence of bright or conspicuous colors or patterns in animals that are toxic, noxious, dangerous, or poisonous to predators. Here’s an example from Wikipedia, the granular poison frog (Oophaga granulifera). Like many dendrobatid frogs, this has a number of poison alkaloids in its skin, and they have been used in Central and South America to tip arrows or darts, which can kill mammals. Any predator that tried to eat one of these would probably be dead, or at least very ill.

My own frog, Atelopus coynei, looks conspicuous too [but see Lou Jost’s comment below], and may be toxic, but I don’t think people know anything about that:

Atelopus coynei. Photo: Jordy Salazar/EcoMinga

But of course far more animals than amphibians are aposematic. The skunk advertises its toxicity with a pair of conspicuous stripes. Many insects, like ladybugs and some leipidopterans, are also aposematic and toxic, including at least one bird species: see here for a Google image search of aposematic animals.

The colors and patterns, as the name implies, gives their bearers an evolutionary advantage over their presumably camouflaged ancestors, for predators will deliberately avoid the pattern, usually because they’ve learned to recognize and stay away from it because of previous unpleasant experiences. (The avoidance can also be evolved rather than learned, as you’ll see if you think about it. Even if eating one of these kills you, individual predators having less of a propensity to attack the pattern would be favored.)  Usually, however, learning is involved.

But to get that advantage, the aposematic species has to be sufficiently numerous to afford predators a chance to learn and then avoid the next aposematic animal. And this creates an evolutionary problem.

We are pretty sure that aposematic species evolved from camouflaged ones. To get the warning coloration started, there have to be mutations in the camouflaged population that produce individuals with bright colors and patterns, at least in incipient form.

And that’s the rub: the first mutant individual stands a higher chance of being attacked and killed than do cryptic individuals. Even if it’s toxic, it may still get killed or injured by being attacked for being a novel, conspicuous creature.  So how does the adaptation ever spread through the population from a rare initial state?

Previously, as described in the excellent Nature News & Views summary by Tim Caro below (click to read), we had a few answers:

1.) The trait could evolved by kin selection in gregarious animals. While the first mutant individual might be attacked, it might be part of a group of relatives that share that aposematic mutation. Assuming the predator learns to avoid the pattern after killing or hurting the first individual, it would avoid its similarly-colored kin, and that is a form of kin selection on the color/pattern genes that could make them spread.

2.) The trait could have evolved from a state that was conspicuous but not as conspicuous as the animals above. But this runs into the same problem as #1!

3.) The attacked aposematic mutant could avoid being killed by the predator because it smells or tastes bad, or is injured only slightly. If the predator learns from one experience (and some do), then that individual would henceforth be protected from predation, perhaps giving the mutant color/pattern gene an advantage. This seems somewhat likely, and could be tested by exposing naive predators to aposematic prey.

4.) Predators might avoid novel colors or patterns in general since the hunters have a search image for edible species. As Caro says, there’s some evidence for this, too.

But now, in his summary of the original paper, Caro describes a fifth hypothesis that is described in the Science paper below that.  The authors test this interesting hypothesis using phylogenetic data, and it seems to be supported.

Click the original Science paper below to read about the novel hypothesis for the evolution of aposematism. The authors test it in amphibians, but may hold for other creatures as well. You can also find the pdf here , and the reference is at the bottom. 

Again, I’ll try to be brief, but may not succeed. The authors’ hypothesis, which is very clever, is that full aposematic coloration may have evolved, at least in amphibians from an earlier state where it wasn’t clearly visible to predators. This could involve the colors/patterns starting their evolution on the BOTTOM (ventral) side of the animal, which wouldn’t draw attention until the animal was attacked, at which point it could flash its pattern and possibly startle the predator (the predator could also learn from a brief encounter that the prey was toxic).  And the bottom-colored state could itself be of two types: small patches on the ventral surface (PV) or a fully colored ventral surface (FV). This is in contrast to an animal that is fully colored all over its body.

Once the predator started learning what the color/pattern means from the animals that had it on their belly, then the color could evolve to cover the animal, making it fully aposematic.

But how do you test this hypothesis? Well, you could see if predators learn to avoid toxic amphibians that had color patches painted on their belly, but there are few amphibians that are toxic and lack aposematic coloration. No, the authors tested their hypothesis by doing phylogenetic reconstruction: they used living species and their known family tree to deduce what the color/pattern of the ancestors were. This kind of reconstruction, which makes sense if you have enough data, is increasingly used to study evolution.

And so Loeffler-Henry et al. did a big reconstruction of the evolutionary history of amphibians, many of whom were aposematically colored. They used 1106 species, putting each in one of five evolutionary categories:

species cryptic (camouflaged; “cry” in photo below)
species PV (ventral side partly aposematic)
species FV (ventral side fully aposematic)
species fully aposematic all over its body (“conspicuous” or “con” in photo below)
species polymorphic (some individuals are aposematic, others not). There aren’t many of these, and I won’t go into why they are supposed to exist.

Here’s a photo from the paper showing four of the five states (a polymorphic species isn’t shown):

Part of paper’s caption: Cry: cryptic; PV (partially conspicuous venter): cryptic dorsum with conspicuous color present as small patches on normally hidden body parts; FV (fully conspicuous venter): cryptic dorsum with conspicuous colors fully covered on the venter; Con: conspicuous

And here’s the reconstruction of the phylogeny showing the position in the family tree of each of the five states. Click to enlarge:

(From paper): Fig. 2. Ancestral state estimation of each color state (N = 1106 species) in frogs and salamanders. Pie charts at each node show the probabilities of ancestral states. The ancestral state of frogs and salamanders is likely to be cryptic coloration. The hidden color signals (PV and FV) are widespread and have evolved multiple times in different lineages. PV: cryptic dorsum with conspicuous color present as small patches on normally hidden body parts; FV: cryptic dorsum with conspicuous colors fully covered on the venter. See table S11 for photo credits.

There’s a pie diagram at each node of the tree showing the probability that that ancestor had one of the five states scored. I won’t go into the methods for deriving probabilities (in truth, I don’t understand them); but her are the salient points:

1.) Ancestors tend to be cryptic (camouflaged; gray dots), with the possible exception of some salamanders. This comports with the evolutionary view that aposematic coloration was not an ancestral condition but evolved as a defensive adaptation to deter predators.

2.) Full aposematism—the orange state—didn’t appear until later in amphibians, and

3.) . . . it did so generally going through an intermediate state of aposematic coloration on the belly (purple and red species)

4.) The preponderance of purple circles earlier than red ones suggests that the condition of full ventral coloration was preceded in time by the evolution of partial ventral coloration: patches of color that could be flashed but are still less conspicuous to predators than fully belly coloration. This suggestion is supported by statistical analysis of the likelihood of the models, but I’ll skip that.

Now this is an analysis of amphibians, but could apply equally well to other species. In fact, many butterflies that have warning coloration have it on their rear wings, which are covered up when they’re resting. It’s only when they fly, or when a predator startles them, that the aposematic coloration is revealed. Here’s an example: an aposematic butterfly from Ray Cannon’s Nature Notes. It’s the common birdwing (Troides helena), known to be very poisonous since the larvae feed on plants containing toxic aristolochic acids.

And here’s a fully aposematic butterfly:

(from site): Altinote dicaeus callianira – its distinct pattern advertises its unpalatability. Photo: Adrian Hoskins

For a long time the evolution of aposematic coloration posed the problem of what evolutionists call an “adaptive valley”: how do you get from one adaptive state (toxic but camouflaged) to a presumably more adapted state (toxic and brightly colored), when the intermediate evolutionary stage (the first mutant individual) was at a disadvantage: mired in an adaptive valley?  This could not occur by natural selecction since selection cannot favor the less adapted (here, “less avoided”) individuals.

The authors propose a solution to this: an adaptive valley wasn’t crossed because the intermediate state—ventral coloration—did confer a selective advantage on the first mutant individuals.

The authors end the paper by suggesting that their scenario could apply to many species; and it well could:

. . . macroevolutionary studies on animal coloration should take into account these underappreciated hidden signals, which are both common and widespread across the animal kingdom, to advance our understanding of the evolution of antipredator defenses. Indeed, many animal taxa such as snakes, fishes, and a variety of arthropods (see fig. S12 for example groups) include species that are cryptic, are aposematic, and have hidden conspicuous signals. We therefore encourage follow-up studies in other taxa to evaluate the generality of the stepping-stone hypothesis as a route to aposematism.

_________________

Loeffler, K., C. Kang, and T. N. Sherratt.  2023. Evolutionary transitions from camouflage to aposematism: Hidden signals play a pivotal role. Science 379:1136-1140. DOI: 10.1126/science.ade5156

Readers’ wildlife photos and story: the gruesome manipulation of hosts by parasites

April 20, 2023 • 9:45 am

Fortuitously, when I hadn’t prepared any posts for today that require my neurons to work, reader Athayde Tonhasca Júnior came through with one of his patented text+photo stories, this time a fascinating one about how opportunistic natural selection can create predator/parasite niches within niches in completely unexpected and astonishing ways. This hierarchy was wonderfully expressed in the short poem “Siphonaptera” (the order in which fleas are placed) by British mathematician Augustus De Morgan:

Great fleas have little fleas upon their backs to bite ’em,
And little fleas have lesser fleas, and so ad infinitum.
And the great fleas themselves, in turn, have greater fleas to go on;
While these again have greater still, and greater still, and so on.

Athayde’s text is indented, and click on the photo to enlarge them.

The body snatchers

by Athayde Tonhasca Júnior

Family feuds abound in history and in the tabloids, but things got really out of hand with the offspring of Egyptian gods Geb (Earth) and Nut (sky). As the first-born, Osiris was naturally chosen to be the ruler of the world. But his brother Set didn’t care one bit for this undemocratic arrangement, so he decided to despatch Osiris to the Underworld. So he set out a murderous plan worthy of an Agatha Christie story. Set first commissioned a beautiful casket, tailored to fit a body with Osiris’ exact measurements. Set then organised a magnificent banquet, inviting heavenly celebrities and bro Osiris. When they were all done with the eating and drinking, Set announced a surprise. The casket was brought in, and the host told his guests that whoever could fit inside, could take it home (an odd gift to us, perhaps, but who are we to judge Egyptian gods?). One by one the guests climbed into the casket, which was too small or too big – until Osiris had a go at it. He laid down inside the casket, which, to his glee, fit him perfectly. Set’s trap was set; he slammed the casket’s lid shut and locked it, killing his sibling. Later Set retrieved Osiris’ body and chopped it into small pieces.

The Mummy (1932) escaped from his sarcophagus, but no such luck for Osiris. Art by Karoly Grosz, Wikimedia Commons:

Set’s shenanigans were the perfect inspiration for naming a new species from the genus Euderus, a small group of parasitic wasps in the family Eulophidae. Most Euderus species are moth and beetle parasitoids, but the wasp discovered by Egan et al. (2017) in Florida (USA) is peculiar, to say the least. Its host, Bassettia pallida, is itself a parasitic wasp, but of a different kind: this species is one of the many gall wasps or cynipids (family Cynipidae), which lay their eggs in oaks (Quercus spp.) and less commonly in related plants (family Fagaceae). The egg-laying induces the plant to produce a gall, which is an abnormal growth resulting from increased size or number of cells (galls can also be caused by tissue feeding or infections by bacteria, viruses, fungi and nematodes). Cynipids trigger their host plants to produce nutritious tissue inside their galls, which become ideal places for a larva to grow: there’s nothing better for one’s survival than a cosy, safe and nourishing nursery.

Oak galls or oak apples, growths resulting from chemicals injected by the larva of gall wasps © Maksim, Wikimedia Commons:

In the case of B. pallida, it induces the formation of galls inside stems of sand live oak (Q. geminata) and southern live oak (Q. virginiana). Each of these galls is called a ‘crypt’. So appropriately, B. pallida is known as the crypt gall wasp. When the adult wasp completes its development, it chews an exit hole from inside its woody quarters and flies away.

(a): a crypt gall wasp; (e): adults’ exit holes © Weinersmith et al., 2020:

Life looked good for the crypt gall wasp in the southeastern United States—until we learned about the machinations of its recently discovered enemy. The Eulophidae parasitoid locates a crypt and pierces it with its ovipositor, laying an egg inside the chamber, near or into the developing crypt gall wasp. We don’t know exactly what goes on inside the chamber, but the outcome is not good at all for the crypt gall wasp. When it tries to chew its way out, it’s no longer able to create a hole big enough to fit its body: the wasp becomes entrapped inside its crypt, Osiris-like. During its failed attempt to get out, its head blocks the exit hole. All the better for the parasitoid larva that hatched inside the crypt: it can feed at leisure on the host’s weakened body. On completing its development, the adult parasitoid wasp chews through the host’s head plug and comes out to the big wide world. So there was no better name for this species than Euderus set, the crypt-keeper wasp.

JAC: Isn’t that an amazing story? I’m sure we don’t know how the parasitoid disables the gall wasp in this way. Imagine the genetic changes involved in this complex evolution, involving the parasitoid’s egg-laying and multiple behaviors of its larval stage. But that’s a passing expression of amazement; let’s continue with Athayde’s tale:

(c): a crypt-keeper wasp pupa in a chamber made by a crypt gall wasp; (f): an exit hole plugged by the head capsule of a dead or dying crypt gall wasp; (g): a crypt gall wasp head capsule chewed through by an exiting crypt-keeper wasp © Weinersmith et al., 2020.

The relationships between oaks and these wasps are examples of host manipulation, which happens when a parasite influences the host’s behaviour or physiology to its (the parasite’s) advantage. The crypt gall wasp induces its host plants to produce galls for its benefit, and in turn the crypt-keeper wasp forces its host into becoming trapped and an easy meal for the parasitoid’s larva: the manipulation of a manipulator is known as a hyper-manipulation, an uncommon phenomenon.

A female crypt-keeper wasp, a hyper-manipulator © Egan et al., Wikimedia Commons.

There are many cases of host manipulation, and the zombie-ant fungus described by the co-author of the theory of evolution by natural selection Alfred Russel Wallace (1823-1913) is one of the better known. This fungus (Ophiocordyceps unilateralis) induces its host ants to climb up the vegetation and clamp their mandibles around a twig or leaf vein. An infected ant will stay put, rain or shine, while the fungus grows inside it. After 4-10 days the ant dies, the fungus grows a ‘stalk’ (stroma) from the ant’s head and releases spores that will infect ants walking about on the forest floor.

A dead Camponotus leonardi ant attached to a leaf vein. The stroma of a zombie-ant fungus emerges from the back of the ant’s head © Pontoppidan et al., 2009:

The more researchers look into it, the more they find cases of host manipulators such as the Darwin wasps Hymenoepimecis spp., which parasitize several species of orb-weaving spiders in the Neotropical region. A female wasp stings and temporarily paralyses her victim, laying an egg on its abdomen. The emerging larva bites through the spider’s cuticle and feeds on its ‘blood’ (haemolymph). The spider carries on with its life, building webs and catching prey, but the growing parasitoid takes its toll; eventually it kills its host.

L: A H. heidyae egg attached to a Kapogea cyrtophoroides. R: Third instar H. heidyae larva feeding on a recently killed spider; the inset shows details of the dorsal hooks used by the larva to cling to its host © Barrantes et al., 2008.

But shortly before the spider’s demise, somehow —probably by hormone injection—the larva takes command of the host’s behaviour. The spider builds a cocoon web made of thickly woven silk, which doesn’t look at all like a normal web. The spider dies, the larva enters the cocoon and completes its development. Some days later, the adult wasp emerges and flies away.

a. A normal K. cyrtophoroides web; b. The web’s hub; c. A cocoon web induced by the parasitoid; d.  Central section of the cocoon web and the wasp’s cocoon © Barrantes et al., 2008.

Parasitic wasps are not deterred by the defences of hosts such as Anelosimus eximius. This is one of the few species of social spiders; they build massive tent-like nests that shelter hundreds or thousands of individuals, who hunt together in raiding packs and even cooperate in raising their young (click the next link to watch their comings and goings). But in the Amazon region, A. eximius can’t evade the Darwin wasp Zatypota sp. A parasitized spider leaves the colony and builds its own cocoon-like web. It then becomes immobilised, so that the wasp larva can unhurriedly consume it. When finished with its meal, the larva enters the cocoon to complete its development. The larger the spider colony, the more chances of being parasitized; up to 2% of individuals become hosts to the parasitoid (Fernandez-Fournier et al., 2018).

L: A group of A. eximius in a communal web © Bernard Dupont, Wikimedia Commons. R: A 5-m long, 3-m high colony of A. eximius; photo by A. Bernard © Krafft & Cookson, 2012:.

A fierce looking H. neotropica and its larva feeding on an Araneus omnicolor © Sobczak et al., 2012.

Host manipulation seems to be much more common than we thought, so we shouldn’t expect pollinators to be safe from it. And they are not. The conopid fly (family Conopidae) Physocephala tibialis forces bumblebee hosts to bury themselves in the soil just before dying. The nematode worm Sphaerularia bombi, found throughout the northern hemisphere and South America, infects queens of several bumble bee species, castrating its host. And at least for the buff-tailed bumble bee (Bombus terrestris), the nematode also alters the bee’s behaviour (Kadoya & Ishii, 2015). An infected queen feeds normally, but does not breed or build a nest. Instead, she keeps flying into the early summer months, and by doing so she unintentionally helps to spread the nematode. Certainly many other cases of pollinators’ manipulation by parasites wait to be discovered because their effects can be subtle and inconspicuous.

CSI Garden: a post-mortem examination of a buff-tailed bumble bee found dying on a roadside pavement in England revealed an infestation by the host-manipulating nematode S. bombi © The Encyclopedia of Life:

Host manipulation can be seen as a form of extended phenotype (Dawkins, 1982; phenotype refers to a species’ observable characteristics resulting from the expression of its genes). By changing the host’s behaviour for its own benefit, the parasitoid – ultimately, its genes – expresses its phenotype in the world at large. In Dawkins’ own words, ‘an animal’s behaviour tends to maximize the survival of the genes “for” that behaviour, whether or not those genes happen to be in the body of the particular animal performing it’. The phenomenon would have deep consequences for natural selection, but the extent of extended phenotypes has been debated since the publication of Dawkins’ book.

If you are smugly assuming that behavioural puppeteering is for lower animals such as insects, you’d better think again. Some studies suggest that rodents infected with the protozoan Toxoplasma gondii become more active but sluggish in reacting to alarm signals; worse, they may become attracted to the smell of cat’s urine. If so, an infected mouse has a good chance of prematurely ending its days in a moggie’s maw – which was T. gondii‘s ‘intention’ all along, since cats are its ultimate host. And the plot thickens: infected cats excrete T. gondii spores in their faeces, which can make their way into other mammals. A 26-year study with grey wolves (Canis lupus) from Yellowstone National Park, Wyoming, USA, revealed that infected individuals – probably the result of contact with pumas (Puma concolor) – are bolder, more likely to become pack leaders and have better chances of reproducing (Meyer et al., 2022). In humans, toxoplasmosis, the infection caused by T. gondii, is widespread but usually does not have any symptoms. Most people don’t even know they have it, but all sorts of behaviour and mental disorders such as heightened aggression and Parkinson’s disease have been linked to the infection. The effects of T. gondii on rodents and humans have been disputed because data often show weak, inconclusive or no effects (Johnson & Koshy, 2020). In any case, our invulnerability to the manipulative power of parasites should not be taken for granted. Rephrasing the quote misattributed to Margaret Mead, always remember that in biology, Homo sapiens is unique. Just like every other species.

Invasion of the Body Snatchers (1956). Art by Allied Artists Pictures Corporation. Wikimedia Commons.

JAC note: I don’t think that in any of these cases of host manipulation (or any others that I’ve heard of) do we know the chemical and developmental basis of the manipulation. What does a fungus do to an ant to make it climb a stalk of grass, grip it tightly with its mandibles, and then die? How does the Darwin wasp manipulate the spider’s behavior to cause it to weave a cocoon-like web instead of its normal web—something good for the wasp? These are incredibly sophisticated manipulations that have evolved in ways we don’t understand.

If this is the work of a creator, he must have been a sadist!